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Macular thickness as determined by optical coherence tomography in relation to degree of myopia, axial length and vitreous chamber depth in Malay subjects Clin Exp Optom 2012; 95: 484–491 Shah Farez Othman*†§ MHSc(Optom) FAMO Sharanjeet-Kaur† PhD Faudziah Abd Manan† PhD Ahmad Iskandar Zulkarnain* MHSc(Optom) Zainal Mohamad§ MS(Ophthal) Azrin E Ariffin* PhD * Faculty of Optometry & Vision Sciences, SEGi University College, Selangor, Malaysia † Optometry & Vision Science Programme, Faculty of Health Sciences, Universiti Kebangsaan Malaysia, Kuala Lumpur, Malaysia § National Institute of Ophthalmic Sciences, Tun Hussein Onn National Eye Hospital, Selangor, Malaysia E-mail: [email protected]

Submitted: 22 July 2011 Revised: 8 December 2011 Accepted for publication: 8 January 2012

DOI:10.1111/j.1444-0938.2012.00752.x Purpose: This study aimed to determine the relationship between macular thickness and spherical equivalent refraction (SER), axial length (AL) and vitreous chamber depth (VCD) in Malay subjects. Methods: Sixty-three subjects (aged 19–24 years) with a mean SER of -1.79 ⫾ 2.24 D, mean axial length of 24.26 ⫾ 1.35 mm and mean vitreous chamber depth of 17.02 ⫾ 1.33 mm were included in this clinical cross-sectional study. Stratus optical coherence tomography (Time Domain optical coherence tomography) was used to determine the thickness of the outer macular (perifovea) and inner macular (parafovea) at four different locations, that is, temporal, superior, nasal and inferior quadrants and also the fovea itself. Results: Positive correlations were found between the outer macular (perifovea) thickness and SER at the temporal (R = 0.47, p < 0.05), superior (R = 0.36, p < 0.05) and inferior (R = 0.31, p < 0.05) quadrants. Foveal thickness was also positively correlated with AL (R = 0.34, p < 0.05) and VCD (R = 0.32, p < 0.05). Negative correlations were found between outer macular thickness and axial length at the temporal (R = -0.46, p < 0.05), superior (R = -0.27, p < 0.05), nasal (R = -0.25, p < 0.05) and inferior (R = -0.36, p < 0.05) quadrants. Negative correlations were also found between outer macular thickness and VCD at the temporal (R = -0.51, p < 0.05), superior (R = -0.32, p < 0.05), nasal (R = -0.31, p < 0.05) and inferior (R = -0.40, p < 0.05) quadrants. Conclusions: This study shows that the degree of myopia and elongation of the globe are associated with thinning of most areas of the perifovea. A trend for foveal thickening in the high myopia group is also inferred, although this does not apply to the low and moderate myopia groups.

Key words: axial length, refraction, macular, myopia, optical coherence tomography, vitreous chamber depth

Myopia is a common condition found in many populations, especially in Asian countries. In Singapore, Hong Kong and Taiwan, the prevalence of high myopia, which is defined as a refractive error of at least -6.00 D, is increasing.1–4 In Malaysia, the prevalence of myopia has been

recorded to be between eight to 50 per cent.5–8 Myopia is a potentially blinding condition owing to its association with ocular disease such as glaucoma, cataract, retinal detachment and degenerative macular neovascularisation.9 In myopic eyes, the globe is enlarged with an

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increase in axial length (AL).10 The stretching of the retina beyond normal dimensions may result in thinning of the retina.11 Retinal changes that occur in highly myopic subjects include peripapillary atrophy, peripheral lattice degeneration, © 2012 The Authors

Clinical and Experimental Optometry © 2012 Optometrists Association Australia

Macular thickness by OCT in Malay myopes Othman, Sharanjeet-Kaur, Manan, Zulkarnain, Mohamad and Ariffin

inclined or malinsertion of the optic disc, posterior staphyloma and breaks in Bruch’s membrane.4,10 Some highly myopic subjects experience several complications that impair visual acuity purely as a result of increased AL or the formation of posterior staphylomata.10 High myopes also tend to have chorioretinal atrophy at the posterior pole,10 choroidal neovascularisation at the macular area12 and a macular hole at the posterior pole.13 Of late, the retinal changes in increasing degrees of myopia have been studied with the technique of optical coherence tomography (OCT). The outer macula (perifovea) has been demonstrated using OCT to be thinner in myopes.14–17 Measurements of the thickness of the inner macula (parafovea) vary in myopic subjects, although similar thinning of this area has been proposed.11,15,17 In contrast, the central fovea has been shown consistently to be thicker in myopic eyes using the technique of OCT.15–19 A study in Singapore on myopic Asian men using 6.0 mm horizontal and vertical linear scans using the OCT Mark I, that is, the first OCT version, showed that the macular thickness at the inner macula was negatively correlated with AL.14 Using the fast macula scan mode on the OCT Mark 3, that is, Stratus OCT, which specifically splits the parafovea into outer macula (perifovea) and inner macula (parafovea) based on the Early Treatment Diabetic Retinopathy Study (EDTRS), the genetic twin study by Chamberlain15 found that the outer macular thickness also correlated negatively with AL. Optical coherence tomographic studies on two Asian adult groups in Japan and Singapore showed that the average macular retinal thickness did not change with increasing myopia.14,20 Conversely, Mrugacz, Bakunowicz-Lazarczyk and Sredzinskakita21 conducted a study in myopic children in Poland and found that the macular thickness (defined as the area consisting of both the fovea and the parafovea) is decreased with increasing myopia. Luo and colleagues11 studied the correlation between OCT macular parameters and ocular biometry in children aged seven to nine years in Singapore and

reported that macular thickness at particular quadrants was reduced except in the inferior and superior quadrants. Lam and colleagues16 studied the relationship between myopia and macular thickness using OCT Mark 3 in Hong Kong and found that the average thickness of the external ring of macula (parafoveal region in OCT Mark I version) in highly myopic eyes (SER greater than -6.00 D) was significantly less than low to moderate (SER -0.50 D to -6.00 D) and non-myopic eyes (SER -0.50 D to +3.50 D). A negative correlation was also found between the AL and the average thickness of the external ring macula.16 Xie and colleagues17 reported similar findings from their study on early adult myopes, where the outer macula in the inferior region was thinner than the other regions of the macula. In contrast, the fovea has been reported to be thicker with increasing myopic refraction and AL.15 When myopia is classified into the categories of low, moderate and high, perifoveal and parafoveal macula thicknesses have been reported16,17 to be least in highly myopic eyes compared to low myopes and emmetropes. These studies also concurrently reported that the fovea was thicker in those with highly myopic eyes. Outer macular thinning is well established in the literature, especially in Chinese eye.17,18 It is expected that being an Asian eye, the Malay eye will experience the same fate, as the prevalence of myopia within the Malay population is similar to rates recorded in the Chinese eye, although not as high.5,8 There is also inconsistency in the literature as to the thickness of the foveal region in myopes.15–17 As it is normally expected that a myope undergoes retinal thinning as a part of myopic progression, it is clinically useful to know whether the fovea or areas surrounding it are undergoing structural alteration. Knowing the exact area(s) undergoing thinning helps the clinician to differentially sort the likely causes of any decrement in the visual acuity of a myopic patient. In such case, if the fovea is the expected ‘thinned area’, then the cause of the fall in visual acuity may be attributable

© 2012 The Authors Clinical and Experimental Optometry © 2012 Optometrists Association Australia

to the fovea itself. Otherwise, if the expected ‘thinned area’ is not the fovea, then the said fall in visual acuity requires the clinician to investigate for other causes. Hence, the present research aimed to document the thickness of the outer and inner macula and their corresponding relationships with the degree of myopia in respect of spherical equivalent refraction (SER), AL and vitreous chamber depth (VCD) in different quadrants of the outer and inner macula, that is, temporal, superior, nasal and inferior regions in a range of Malay myopic eyes. The foveal thickness and its relationship with the degree of myopia, both in respect of SER and linear dimensions of the eyeball were also sought.

MATERIALS AND METHODS One randomly selected eye of consecutive ophthalmologically normal Malay subjects with refractive errors that lay within emmetropia and a certain defined range of myopia was included. The work was carried out at the National Institute of Ophthalmic Sciences, Tun Hussein Onn National Eye Hospital (THONEH), Petaling Jaya. Inclusion criteria were based on the age range of 19 to 24 years, visual acuity (VA) of 6/6 or better and N6, SER ranging between +0.75 D and -8.00 D and intraocular pressure (IOP) no greater than 22 mmHg. The age range of 19 to 24 was selected to ensure the maturity of ocular component growth22–24 and to exclude age-related changes in the macula.18 Subjects were free of ocular and systemic pathology with open anterior chamber angles. Exclusion criteria were: a history of intraocular or refractive surgery, glaucoma, retinal disease, current treatment that could change the IOP and retinal thickness, anisometropia of more than 0.50 D, astigmatism of more than 1.00 D and other neurological diseases. Eyes with any abnormal OCT findings, that is, those with signal strength less than eight and decentered images were also excluded.


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A

B

C2 B2

C1

B1

A

B3

C3

B4 C4

Figure 1. Fast macular scan protocol by optical coherence tomography (OCT) of the right eye, which consists of 6.0 mm radial scans 30° apart (A). The OCT scanning image with resulting macular thickness is shown (B). Three concentric circles are formed 1.0, 3.0 and 6.0 mm in diameter around the central point of the fovea (A). The area marked A is the fovea (1.0 mm); areas from B1 to B4 (temporal to inferior) are the four quadrants of the inner macula ring (parafovea) and areas from C1 to C4 are the four quadrants of the outer macula ring (perifovea).

Data were collected from June 2006 to November 2007 at the optometry and ophthalmology clinics at THONEH. This research was approved by the Research and Ethics Committee for Medical Research (FF-239-2007), National University of Malaysia and complied with the tenets of the Declaration of Helsinki. Informed consent was obtained from each subject before enrolment. All subjects underwent evaluation of VA, slitlamp examination of the anterior segment, tonometry, cycloplegic refraction, fundus photography, A-scan ultrasound and Stratus OCT 3000 examination. During cycloplegic refraction, retinoscopy was performed and recorded as spherical equivalent refraction and then classified as emmetropia (SER between +0.50 D and -0.50 D), low myopia (SER from -0.75 D to -2.00 D), moderate myopia (SER from -2.25 D to -6.00 D) or high myopia (SER greater than -6.00 D). Detailed information on OCT imaging is described in the Stratus OCT manual 3000.25 Data are presented in figures and false-colour topographic maps. The

computer software analyses the image automatically. In the present study, the Stratus OCT Mark 3 (Carl Zeiss Meditec, Dublin, CA, USA) was used to measure retinal thickness of the macula (within a 6.0 mm diameter). Two reticules were used to divide each ring into four quadrants (temporal, nasal, superior and inferior). The Fast Macular Scan protocol was used to scan the entire thickness of the retina in the macular area. The scan consisted of a 6.0 mm radial line at six meridians, which formed patterns of clock hours. Each radial line consisted of 128 A-scans and a total number of 768 A-scan patterns were completed in less than two seconds. The profile of retinal thickness was taken from each cross-sectional image. The selected cross-sectional OCT image was presented with clear overlapping boundaries within and outside of the retina-based image processing software. Retinal thickness profiles from the six cross-sectional images were interpolated using a colour scale forming the retinalmacula thickness map. All scanning results


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were automatically analysed by the Version 4.1 software, which also measured the thickness of the retina from the inner limiting membrane to the junction of the photoreceptor inner and outer segments. The instrument was centred on the foveal pit and the macula was automatically divided into three concentric rings: centre, inner and outer rings (1.0, 3.0 and 6.0 mm diameter, respectively, Figure 1). The centre, inner and outer rings represented the foveal, inner (parafovea) and outer macular (perifovea) areas, respectively. All data were analysed using the statistical package SPSS version 14.0 for windows (SPSS Inc., Chicago, IL, USA). A p-value of less than 0.05 was considered statistically significant. RESULTS Sixty-three eyes of 63 Malay subjects (27 male and 36 female) enrolled in the study were available for analysis. There were 14 subjects categorised as low myopia, that is, with SER of -1.94 ⫾ 0.63 D, 13 being in the moderate myopia category with SER of -4.22 ⫾ 0.98 D and four in the high myopia group with SER of -7.22 ⫾ 0.66 D. Thirty-two emmetropic subjects, that is, with SER -0.06 ⫾ 0.28 D were also recruited. All subjects had a mean age of 20.7 ⫾ 1.3 years ranging from 19 to 24 years. The mean SER of all subjects was -1.79 ⫾ 2.24 D (range: +0.50 to -8.00 D), the mean AL was 24.26 ⫾ 1.35 mm (range: 21.88 to 30.14 mm) and the mean VCD was 17.02 ⫾ 1.33 mm (range: 15.10 to 23.26 mm). The SER was significantly correlated to AL (R = -0.71, p < 0.05) and VCD (R = -0.69, p < 0.05). Fast ‘macular thickness’ OCT scans from two subjects in the study, namely an emmetrope and a myope are shown in Figure 2. Foveal and regional macular thickness measurements in each group are summarised in Table 1. There were no significant inter-group differences in the foveal thickness and in the thickness of all the inner rings of the macula (p > 0.05). There were significant differences in the mean outer macular thickness between the myopic groups and the © 2012 The Authors

Clinical and Experimental Optometry © 2012 Optometrists Association Australia


EMMETROPE (SER = 0.25 D)

MYOPE (SER = -4.75 D)

ILM IS/OS

ILM IS/OS

A-Scan value

A-Scan value

Microns

Microns

Thickness chart

600

600

500

500

400

400

300

300

200

200

100

Thickness chart

100 A-scan

0 0

10

20

30

40

50

60

70

80

90

100 110 120

A-scan

0 0

10

20

30

40

50

60

70

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100 110 120

Figure 2. Fast macular thickness optical coherence tomography scan from an emmetrope (left) and a myope (right). Retinal thickness is measured anteriorly, from the inner limiting membrane (ILM) to the junction of the photoreceptor inner and outer segments (IS/OS) posteriorly.

Optical coherence tomography measurement

Controls (n = 32)

Low myopes (n = 14)

Moderate myope (n = 13)

High myopes (n = 4)

p-value

Macular thickness (mm) Fovea

186.91 ⫾ 19.39

177.64 ⫾ 12.77

187.62 ⫾ 19.80

206.00 ⫾ 24.10

0.06

Inner temporal

263.25 ⫾ 15.17

256.86 ⫾ 11.10

263.23 ⫾ 14.15

250.50 ⫾ 12.48

0.21

Inner superior

274.78 ⫾ 16.07

268.71 ⫾ 10.85

277.46 ⫾ 14.64

264.75 ⫾ 10.59

0.25

Inner nasal

275.13 ⫾ 17.38

266.29 ⫾ 13.80

278.92 ⫾ 15.45

269.50 ⫾ 15.28

0.20

Inner inferior

275.03 ⫾ 15.87

267.64 ⫾ 9.87

274.38 ⫾ 12.50

259.75 ⫾ 12.92

0.11

Outer temporal

226.69 ⫾ 12.80

218.14 ⫾ 9.16

219.31 ⫾ 11.00

203.75 ⫾ 10.21